Abstract
Mycobacterium is an interesting genus which not only includes intimidating pathogens, associated with severe devastations globally, but also comprises of non-pathogenic eco-friendly members that detoxify environmental pollutants. Secretory proteins of the mycobacterial communities are essential components which are firmly believed to facilitate proper cross-talk and apt communication with host cellular surroundings and environmental niche. Secretory elements also play vital roles in mycobacterial pathogenesis. In the present endeavor, an extensive profiling of mycobacterial secretomes, considering both pathogenic and non-pathogenic members, has been executed. Thorough analysis on amino acid composition and functional behavior of the mycobacterial secretory proteins has also been performed. In-depth scrutiny of biosynthetic cost of the secretory proteins with respect to the non-secretory ones indicated that the genus Mycobacterium strictly follows the policy of cost-minimization among the sets of imperative secretory proteins. Comprehensive assessment of potential virulence among the key secretory components signified that the pathogenic mycobacterial members possess a larger share of potentially virulent secretory elements in comparison to their non-pathogenic counterparts. Present analysis also revealed contrasted evolutionary features of the secretomes wherein secretory proteins were found to evolve faster than non-secretory proteins in mycobacterial pathogens but not in the concerned non-pathogens. Outcomes of present investigation promise to provide novel insights into the enigma of mycobacterial pathogenesis, bioremediation and adaptation in diverse niche and aid further scientific investigations associated with concerned research area.
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Change history
04 January 2021
Unfortunately, in the published paper entitled "Comprehensive profiling of functional attributes, virulence potential and evolutionary dynamics in mycobacterial secretomes" authored by Ayan Roy, Arnab Sen, Sourav Chakraborty and Indrani Sarkar, the surname of Sourav Chakraborty was inadvertently wrongly written as Sourav Chakrobarty in the original publication of the article. Name has been corrected in the correction article. We have also included ORCID ID.
References
Akashi H, Gojobori T (2002) Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 99:3695–3700
Bendtsen JD, Kiemer L, Fausbøll A, Brunak S (2005a) Non-classical protein secretion in bacteria. BMC Microbiol 5:58
Bendtsen JD, Nielsen H, Widdick D, Palmer T, Brunak S (2005b) Prediction of twin-arginine signal peptides. BMC Bioinformatics 6:167
Brosch R, Gordon SV, Eiglmeier K, Garnier T, Cole ST (2000) Comparative genomics of the leprosy and tubercle bacilli. Res Microbiol 151:135–142
Buggiotti L, Primmer CR (2006) Molecular evolution of the avian growth hormone gene and comparison with its mammalian counterpart. J Evol Biol 19:844–854
Champion PA, Cox JS (2007) Protein secretion systems in Mycobacteria. Cell Microbiol 9:1376–1384
Chen L, Yang J, Yu J, Yao Z, Sun L, Shen Y et al (2005) VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 33:D325–D328
Choo SW, Dutta A, Wong GJ, Wee WY, Ang MY, Siow CC (2016) Comparative genomic analysis reveals a possible novel non-tuberculous Mycobacterium species with high pathogenic potential. PLoS ONE 11:e0150413
Coleman NV, Yau S, Wison NL, Nolam LM, Migocki MD, Ly MA et al (2011) Untangling the multiple monooxygenases of Mycobacterium chubuense strain NBB4, a versatile hydrocarbon degrader. Environ Microbiol Rep 3:297–307
Cornejo-Granados F, Zatarain-Barrón ZL, Cantu-Robles VA, Mendoza-Vargas A, Molina-Romero C, Sánchez F et al (2017) Secretome prediction of two M. Tuberculosis clinical isolates reveals their high antigenic density and potential drug targets. Front Microbiol 8:128
Das S, Pettersson BM, Behra PR, Ramesh M, Dasgupta S, Bhattacharya A et al (2015) Characterization of three Mycobacterium spp. with potential use in bioremediation by genome sequencing and comparative genomics. Genome Biol Evol 7:1871–1886
Demangel C, Stinear TP, Cole ST (2009) Buruli ulcer: reductive evolution enhances pathogenicity of Mycobacterium ulcerans. Nat Rev Microbiol 7:50–60
Eiglmeier K, Parkhill J, Honoré A, Garnier T, Tekaia F, Telenti A et al (2001) The decaying genome of Mycobacterium leprae. Lepr Rev 72:387–398
Embley TM, Stackebrandt E (1994) The molecular phylogeny and systematics of the actinomycetes. Annu Rev Microbiol 48:257–289
Foster SC, Schneider B, Seaman WB (1970) Gas-containing pyogenic intrahepatic abscesses. Radiology 94:613–618
Frothingham R, Hills HG, Wilson KH (1994) Extensive DNA sequence conservation throughout the Mycobacterium tuberculosis complex. J Clin Microbiol 32:1639–1643
Garg A, Gupta D (2008) VirulentPred: a SVM based prediction method for virulent proteins in bacterial pathogens. BMC Bioinformatics 9:62
Gomez M, Johnson S, Gennaro ML (2000) Identification of secreted proteins of Mycobacterium tuberculosis by a bioinformatic approach. Infect Immun 68:2323–2327
Gomez A, Mve-Obiang A, Vray B, Rudnicka W, Shamputa IC, Portaels F et al (2001) Detection of phospholipase C in nontuberculous mycobacteria and its possible role in hemolytic activity. J Clin Microbiol 39:1396–1401
Graur D, Li WH (2002) Fundamentals of molecular evolution. Sinauer Associates Inc., Sunderland
Green ER, Mecsas J (2016) Bacterial secretion systems: an overview. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.VMBF-0012-2015
Hegde RS (2002) Targeting and beyond: new roles for old signal sequences. Mol Cell 10:697–698
Horsburgh CR Jr (1991) Mycobacterium avium complex infection in the acquired immunodeficiency syndrome. N Engl J Med 324:1332–1338
Hsiao WW, Ung K, Aeschliman D, Bryan J, Finlay BB, Brinkman FS (2005) Evidence of a large novel gene pool associated with prokaryotic genomic islands. PLoS Genet 1:e62
Imaeda T (1985) Deoxyribonucleic acid relatedness among selected strains of Mycobacterium tuberculosis, Mycobacterium bovis, Mycobacterium bovis BCG, Mycobacterium microti, and Mycobacterium africanum. Int J Syst Evol Microbiol 35:147–150
Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12:1652–1662
Käll L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction—the Phobius web server. Nucleic Acids Res 35:W429–W432
Kim SJ, Kweon O, Jones RC, Freeman JP, Edmondson RD, Cerniglia CE (2007) Complete and integrated pyrene degradation pathway in Mycobacterium vanbaalenii PYR-1 based on systems biology. J Bacteriol 189:464–472
Koeck JL, Fabre M, Simon F, Daffé M, Garnotel E, Matan AB et al (2011) Clinical characteristics of the smooth tubercle bacilli ‘Mycobacterium canettii’ infection suggest the existence of an environmental reservoir. Clin Microbiol Infect 17:1013–1019
Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Leversen NA, de Souza GA, Målen H, Prasad S, Jonassen I, Wiker HG (2009) Evaluation of signal peptide prediction algorithms for identification of mycobacterial signal peptides using sequence data from proteomic methods. Microbiology 155:2375–2383
Li YD, Xie ZY, Du YL, Zhou Z, Mao XM, Lv LX et al (2009) The rapid evolution of signal peptides is mainly caused by relaxed selection on non-synonymous and synonymous sites. Gene 436:8–11
Malen H, Berven FS, Fladmark KE, Wiker HG (2007) Comprehensive analysis of exported proteins from Mycobacterium tuberculosis H37Rv. Proteomics 7:1702–1718
Marjanovic O, Miyata T, Goodridge A, Kendall LV, Riley LW (2010) Mce2 operon mutant strain of Mycobacterium tuberculosis is attenuated in C57BL/6 mice. Tuberculosis (Edinb) 90:50–56
Mattow J, Schaible UE, Schmidt F, Hagens K, Siejak F, Brestrich G et al (2003) Comparative proteome analysis of culture supernatant proteins from virulent Mycobacterium tuberculosis H37Rv and attenuated M. bovis BCG Copenhagen. Electrophoresis 24:3405–3420
McNally L, Viana M, Brown SP (2014) Cooperative secretions facilitate host range expansion in bacteria. Nat Commun 5:4594
Miller CD, Hall K, Liang YN, Nieman K, Sorensen D, Issa B et al (2004) Isolation and characterization of polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates from soil. Microb Ecol 48:230–238
Mostowy S, Onipede A, Gagneux S, Niemann S, Kremer K, Desmond EP et al (2004) Genomic analysis distinguishes Mycobacterium africanum. J Clin Microbiol 42:3594–3599
Mueller PS, Edson RS (2001) Disseminated Mycobacterium abscessus infection manifesting as fever of unknown origin and intra-abdominal lymphadenitis: case report and literature review. Diagn Microbiol Infect Dis 39:33–37
Nogueira T, Touchon M, Rocha EP (2012) Rapid evolution of the sequences and gene repertoires of secreted proteins in bacteria. PLoS ONE 7:e49403
Pallen MJ, Chaudhuri RR, Henderson IR (2003) Genomic analysis of secretion systems. Curr Opin Microbiol 6:519–527
Peden JF (2000) Analysis of codon usage. Dissertation, The University of Nottingham, UK
Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786
Pintar J, Starmer WT (2003) The costs and benefits of killer toxin production by the yeast Pichia kluyveri. Antonie Van Leeuwenhoek 83:89–97
Prasanna AN, Mehra S (2013) Comparative phylogenomics of pathogenic and non-pathogenic Mycobacterium. PLoS ONE 8:e71248
Rahman SA, Singh Y, Kohli S, Ahmad J, Ehtesham NZ, Tyagi AK et al (2014) Comparative analyses of nonpathogenic, opportunistic, and totally pathogenic mycobacteria reveal genomic and biochemical variabilities and highlight the survival attributes of Mycobacterium tuberculosis. MBio 5:e02020
Ranganathan S, Garg G (2009) Secretome: clues into pathogen infection and clinical applications. Genome Med 1:113
Roy A, Bhattacharya S, Bothra AK, Sen A (2013) A database for Mycobacterium secretome analysis: ‘MycoSec’ to accelerate global health research. Omics 17:502–509
Saier MH Jr (1994) Protein uptake into E. coli during Bdellovibrio infection. A process of reverse secretion? FEBS Lett 337:14–17
Saier MH Jr (2006) Protein secretion and membrane insertion systems in gram-negative bacteria. J Membr Biol 214:75–90
Saini V, Raghuvanshi S, Khurana JP, Ahmed N, Hasnain SE, Tyagi AK et al (2012) Massive gene acquisitions in Mycobacterium indicus pranii provide a perspective on mycobacterial evolution. Nucleic Acids Res 40:10832–10850
Seligmann H (2003) Cost-minimization of amino acid usage. J Mol Evol 56:151–161
Smith DR, Chapman MR (2010) Economical evolution: microbes reduce the synthetic cost of extracellular proteins. MBio 1:e00131-10
Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV et al (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41
Thakur S, Normand P, Daubin V, Tisa LS, Sen A (2013) Contrasted evolutionary constraints on secreted and non-secreted proteomes of selected Actinobacteria. BMC Genom 14:474
Tjalsma H, Antelmann H, Jongbloed JD, Braun PG, Darmon E, Dorenbos R et al (2004) Proteomics of protein secretion by Bacillus subtilis: separating the “secrets” of the secretomes. Microbiol Mol Biol Rev 68:207–233
Vargas-Romero F, Guitierrez-Najera N, Mendoza-Hernández G, Ortega-Bernal D, Hernández-Pando R, Castañón-Arreola M (2016) Secretome profile analysis of hypervirulent Mycobacterium tuberculosis CPT31 reveals increased production of EsxB and proteins involved in adaptation to intracellular lifestyle. Pathog Dis 74:flv127
Vesth T, Lagesen K, Acar O, Ussery D (2013) CMG-biotools, a free workbench for basic comparative microbial genomics. PLoS ONE 8:e60120
Vizcaíno C, Restrepo-Montoya D, Rodríguez D, Niño LF, Ocampo M, Vanegas M et al (2010) Computational prediction and experimental assessment of secreted/surface proteins from Mycobacterium tuberculosis H37Rv. PLoS Comput Biol 6:e1000824
von Heijne G (1990) The signal peptide. J Membr Biol 115:195–201
Wagner A (2005) Energy constraints on the evolution of gene expression. Mol Biol Evol 22:1365–1374
Wang J, McIntosh F, Radomski N, Dewar K, Simeone R, Enninga J et al (2015) Insights on the emergence of Mycobacterium tuberculosis from the analysis of Mycobacterium kansasii. Genome Biol Evol 7:856–870
Willumsen PA, Nielsen JK, Karlson U (2001) Degradation of phenanthrene-analogue azaarenes by Mycobacterium gilvum strain LB307T under aerobic conditions. Appl Microbiol Biotechnol 56:539–544
Wu TS, Chiu CH, Yang CH, Leu HS, Huang CT, Chen YC et al (2012) Fish tank granuloma caused by Mycobacterium marinum. PLoS ONE 7:e41296
Xia X (2013) DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol 30:1720–1728
Zakham F, Aouane O, Ussery D, Benjouad A, Ennaji MM (2012) Computational genomics-proteomics and Phylogeny analysis of twenty one mycobacterial genomes (Tuberculosis & non Tuberculosis strains). Microb Inform Exp 2:7
Acknowledgements
The authors acknowledge the Department of Biotechnology, Government of India, for providing financial assistance in setting up of Bioinformatics Infrastructural Facility (BIF) at University of North Bengal. AS acknowledges the grant received from Department of Biotechnology, Govt. of West Bengal (Project No. 206/BT-Estt./RD-22/2014). AR acknowledges CSIR for providing financial assistance during execution of the work. IS acknowledges the receipt of UGS-BSR fellowship.
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The funding was provided by Department of Biotechnology, Government of India, Department of Biotechnology, Government of West Bengal, India (Project No. 206/BT-Estt./RD-22/2014), Council of Scientific and Industrial Research and University Grants Commission.
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The Original online version of this article was revised: Author name “Sourav Chakraborty” has been corrected.
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Roy, A., Sen, A., Chakraborty, S. et al. Comprehensive profiling of functional attributes, virulence potential and evolutionary dynamics in mycobacterial secretomes. World J Microbiol Biotechnol 34, 5 (2018). https://doi.org/10.1007/s11274-017-2388-1
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DOI: https://doi.org/10.1007/s11274-017-2388-1